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The Shape of the ACC Contributes to Cognitive Control Efficiency in Preschoolers

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The Shape of the ACC Contributes to Cognitive Control Efficiency in Preschoolers The Shape of the ACC Contributes to Cognitive Control Efficiency in Preschoolers Arnaud Cachia1,2*, Grégoire Borst1,2*, Julie Vidal1,2, Clara Fischer3, Arlette Pineau4, Jean-François Mangin3, and Olivier Houdé1,2,5 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/26/1/96/1780446/jocn_a_00459.pdf by MIT Libraries user on 17 May 2021 Abstract ■ Cognitive success at school and later in life is supported by lower Stroop interference scores for both RTs and error rates, executive functions including cognitive control (CC). The pFC in children with asymmetrical ACC sulcal pattern (i.e., different plays a major role in CC, particularly the dorsal part of ACC or pattern in each hemisphere) compared with children with sym- midcingulate cortex. Genes, environment (including school cur- metrical pattern (i.e., same pattern in both hemispheres). Criti- ricula), and neuroplasticity affect CC. However, no study to date cally, ACC sulcal pattern had no effect on performance in the has investigated whether ACC sulcal pattern, a stable brain feature forward and backward digit span tasks suggesting that ACC sulcal primarily determined in utero, influences CC efficiency in the pattern contributes to the executive ability to resolve conflicts early stages of cognitive and neural development. Using anatom- but not to the ability to maintain and manipulate information in ical MRI and three-dimensional reconstruction of cortical folds, working memory. This finding provides the first evidence that we investigated the effect that ACC sulcal pattern may have on preschoolersʼ CC efficiency is likely associated with ACC sulcal the Stroop score, a classical behavioral index of CC efficiency, in pattern, thereby suggesting that the brain shape could result in 5-year-old preschoolers. We found higher CC efficiency, that is, early constraints on human executive ability. ■ INTRODUCTION conflict condition, typically results in increased RTs and Cognitive control (CC) including inhibitory control—that error rates (ERs) because of the need to inhibit irrelevant is, the ability to overcome conflicts and inhibit a dominant stimulus feature (i.e., the color denoted by the word) to response—is one of the core executive functions that focus on an alternative feature of the stimulus (i.e., the enable us to resist habits or automatisms, temptations, ink color). The Stroop interference score reflect the ability distractions, or interference and allow us to adapt to of CC to overcome perceptual and cognitive conflicts complex situations by means of mental flexibility, namely, through the inhibition of a dominant response, namely dynamic inhibition/activation of competing cognitive reading when verbal material is presented (MacLeod, strategies (Diamond, 2013). The Stroop Color–Word task 1991). However, the Stroop Color–Word task involves (Stroop, 1935) is a seminal task designed to assess the other cognitive processes, such as selective attention, con- ability to process conflicting information, drawing, in part, flict monitoring, perceptual, semantic interference, re- on CC. In the classical Stroop Color–Word task, par- sponse interference, and working memory (MacLeod, ticipants are instructed to name the color of the ink of Dodd, Sheard, Wilson, & Bibi, 2003). Functional brain- printed words that denote colors. In the no-conflict con- imaging studies (Roberts & Hall, 2008; Matthews, Paulus, dition, the ink colors match the colors denoted by the Simmons, Nelesen, & Dimsdale, 2004; Bush, Luu, & words (e.g., “RED” appears in red ink), whereas in the Posner, 2000; Casey et al., 2000; Pardo, Pardo, Janer, & conflict condition, the colors denoted by the words inter- Raichle, 1990) have demonstrated that the medial pFC fere with the ink colors to be named (e.g., “RED” appears and more precisely the dorsal ACC, also referred to as the in blue ink). The conflict condition, in contrast to the no- midcingulate cortex (Vogt, 2009), is consistently activated in Stroop tasks (Petersen & Posner, 2012) and other tasks that involve overriding prepotent responses, selecting re- sponses in underdetermined contexts, or errors (Petersen 1CNRS U3521, Laboratory for the Psychology of Child Devel- & Posner, 2012). According to the conflict-monitoring opment and Education, Sorbonne, Paris, France, 2Université Paris Descartes, Paris, France, 3Computer-Assisted Neuroimaging hypothesis (Botvinick, 2007; Botvinick, Braver, Barch, Laboratory, Neurospin, I2BM, CEA, Gif/Yvette, France, 4Université Carter, & Cohen, 2001), one of the core functions of the Caen Basse Normandie, Caen, France, 5Institut Universitaire de dorsal ACC is to signal conflict in information processing France, Paris, France to the CC system supported through dorsolateral prefrontal *These authors contributed equally to this work. cortices. To resolve this conflict, the CC system increases © 2013 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 26:1, pp. 96–106 doi:10.1162/jocn_a_00459 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00459 by guest on 28 September 2021 the activation of task-relevant information and inhibits Guerrini, Kuzniecky, Jackson, & Dobyns, 2012; Rakic, task-irrelevant information (see Egner & Hirsch, 2005). 2004; Molko et al., 2003; Dehay, Giroud, Berland, Killackey, From a developmental psychology perspective, ex- & Kennedy, 1996). As opposed to quantitative measures ecutive functions including CC are known to support of the cortex morphology, such as the Gyrification Index qualities such as self-control, creativity, and reasoning (Zilles, Palomero-Gallagher, & Amunts, 2013; White, Su, that children require to be successful in school and later Schmidt, Kao, & Sapiro, 2010; Armstrong, Schleicher, in life (Diamond, 2013). Executive function efficiency is a Omran, Curtis, & Zilles, 1995) or cortex structure, such better predictor of school readiness and future academic as the thickness, surface, and volume (Giedd et al., 2009; success than intelligence quotient (Blair & Razza, 2007; Gogtay et al., 2004), that vary from childhood through Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/26/1/96/1780446/jocn_a_00459.pdf by MIT Libraries user on 17 May 2021 Duckworth & Seligman, 2005). Given the critical role early adulthood, the sulcal pattern, a qualitative measure that executive functions play in academic achievement, of the cortex morphology, is a stable feature of the brain numerous studies have focused on how to improve anatomy apparently less affected by brain maturation, executive function efficiency. Diverse activities seem training, and learning occurring after birth (Sun et al., to increase executive function efficiency (Diamond & 2012). Two types of ACC sulcal pattern (Ono, Kubik, & Lee, 2011), including school curricula (Diamond, Barnett, Abarnathey, 1990) are defined between 10 and 15 weeks Thomas, & Munro, 2007), attention training (Rueda, of fetal life (White et al., 2010): the “single” type, with Rothbart, McCandliss, Saccomanno, & Posner, 2005), only the cingulate sulcus, and the “double parallel” type, computerized training (Holmes, Gathercole, & Dunning, with an additional paracingulate sulcus (PCS; Paus et al., 2009), noncomputerized games (Mackey, Hill, Stone, & 1996). Recent functional data indicate that participants Bunge, 2011), aerobics (Hillman, Erickson, & Kramer, without a PCS do not lack a particular cortical area, that 2008), martial arts (Lakes & Hoyt, 2004), yoga, and mindful- is, “single” and `“double parallel” ACC types are homolo- ness (Flook et al., 2010). For instance, Tools of the Mind— gous cortical regions (Amiez et al., 2013). The “double a school curriculum for preschool kindergarten that empha- parallel” is observed in 30–60% of individuals, and this sizes imaginary play—improves executive functions to a ACC type is more frequent in the left hemisphere (Yucel larger extent than high-quality school curricula based on et al., 2001). In adults, asymmetry in the sulcal pattern of literacy and thematic units (Diamond et al., 2007). ACC (i.e., the “single” type in the left hemisphere and From a neuroscience perspective, studies have demon- the “double parallel” type in the right hemisphere or vice strated that prolonged learning and specific trainings— versa) is associated with increased CC efficiency (Huster, leading to the improvement of cognitive efficiency—can Westerhausen, & Herrmann, 2011; Fornito et al., 2004) modify the structure (e.g., gray matter volume, cortical and the increased efficiency to manage cognitive conflicts thickness) of brain areas functionally related to the pro- and inhibit dominant responses as measured by the per- cesses trained (Hyde et al., 2009; Draganski et al., 2004, formance in a Stroop Color–Word task at the behavioral 2006). For example, adults who learned to juggle over and electrophysiological level (Huster, Enriquez-Geppert, a 3-month period present an increase of the gray matter Pantev, & Bruchmann, 2012; Huster et al., 2009). However, volume in the visual motion area. The increase of the gray no study to date has investigated whether the sulcal matter volume reveals one of the neuroplasticity mecha- pattern of ACC already affects CC efficiency in the early nisms mediating the improvement of cognitive ability stages of cognitive and neural development. following intense training (Draganski et al., 2004). This is In our study, using anatomical MRI, we investigated not limited to the motor domain; studies have demon- whether an early neurodevelopmental constraint—that
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